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ISSN 1519-6984 (Print)

ISSN 1678-4375 (Online)

THE INTERNATIONAL JOURNAL ON NEOTROPICAL BIOLOGY


THE INTERNATIONAL JOURNAL ON GLOBAL BIODIVERSITY AND ENVIRONMENT

Original Article

Impact of a large dam on reproduction of a non-migratory


teleost species, Acestrorhynchus lacustris (Characiformes:
Acestrorhynchidae)
Impacto de uma grande barragem na reprodução de uma espécie de teleósteo não
migradora, Acestrorhynchus lacustris (Characiformes: Acestrorhynchidae).

R. Z. Gomesa , A. L. Paschoalinia , A. A. Weberb , K. B. Santiagoc , E. Rizzod  and N. Bazzolia* 


a
Pontifícia Universidade Católica de Minas Gerais – PUC Minas, Instituto de Ciências Biológicas e da Saúde, Programa de Pós-graduação em Biologia
de Vertebrados, Belo Horizonte, MG, Brasil
b
University of California, Department of Pharmacology, Robert Tukey Lab, San Diego, CA, United States
c
Centro Integrado de Recursos Pesqueiros e Aquicultura de Três Marias – CODEVASF, Três Marias, MG, Brasil
d
Universidade Federal de Minas Gerais – UFMG, Instituto de Ciências Biológicas, Departamento de Morfologia, Laboratório de Ictiohistologia, Belo
Horizonte, MG, Brasil

Abstract
The release of water from the reservoir hypolimnion, lower concentration of oxygen and the anthropogenic
regulation of the river flow, could affect the reproduction of fish, especially migratory species. However, little is
known about the effects of these changes in water on non-migratory species. In this sense, the reproduction of
Acestrohynchus lacustris was evaluated in two sections of São Francisco River, Minas Gerais, Brazil. Section 1, located
immediately downstream from Três Marias Dam (18°09’31.65”S and 45°13’36.00”W) and section 2, located at the
confluence of the São Francisco and the Abaeté Rivers (18°02’47.78”S and 45°10’57.95”W). For this, we obtained the
physico-chemical parameters of water of each study section. Additionally, biometric data and biological indices of
all specimens were measured. Fecundity and follicles diameters were measured in females. Temperature, dissolved
oxygen and flow showed lower values in section 1. Fish captured in this section, had lower values of GSI in both
sexes, and females presented decreased values of fecundity and follicles diameter. This species showed reproductive
activity in the two sections analyzed, however, in section 1 where the temperature and dissolved oxygen presented
significant lower values, the reproductive capacity of A. lacustris, was negatively affected.
Keywords: hypolimnion, fecundity, dogfish, neotropical fish, Três Marias Dam.

Resumo
A liberação de água do hipolímnio do reservatório, baixa concentração de oxigênio e a regulação antropogênica
do fluxo do rio podem afetar a reprodução de peixes, principalmente espécies migradoras. No entanto, pouco
se sabe sobre os efeitos dessas mudanças nas condições da água em espécies não migradoras. A reprodução de
Acestrohynchus lacustris foi avaliada em duas seções do rio São Francisco. Seção 1, localizada imediatamente a jusante
da barragem de Três Marias e seção 2, localizada na confluência dos rios São Francisco e Abaeté. Para isso, foram
obtidos os parâmetros físico-químicos da água de cada seção do estudo. Além disso, dados biométricos e índices
biológicos de todos os peixes capturados foram obtidos. Adicionalmente, nas fêmeas foram medidos os diâmetros
dos folículos vitelogênicos e a fecundidade. Temperatura, oxigênio dissolvido e fluxo apresentaram valores mais
baixos na seção 1. Os peixes capturados nesta seção apresentaram menores valores de IGS em ambos os sexos, e as
fêmeas apresentaram menores valores de fecundidade e diâmetro dos folículos. Essa espécie apresentou atividade
reprodutiva nas duas seções analisadas, porém, na seção 1, onde os parâmetros da água apresentam piores condições
para o processo reprodutivo de peixes, a capacidade reprodutiva de A. lacustris foi afetada negativamente.
Palavras-chave: hipolímnio, fecundidade, peixe-cachorro, peixes neotropicais, Barragem de Três Marias.

1. Introduction

River damming is considered one of the main impacts anthropogenic regulation of the natural flow of the river,
on riverine ecosystems due to the alteration in physical thus influencing the reproduction and behaviour of fishes
and chemical parameters of the water, as well the (Cetra and Petrere Junior, 2006; Agostinho et al., 2008;

*e-mail: bazzoli@pucminas.br
Received: July 13, 2020 – Accepted: November 4, 2020
This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.

Brazilian Journal of Biology, 2022, vol. 82, e240894  |  https://doi.org/10.1590/1519-6984.240894 1/9


Gomes, R.Z. et al.

Abujanra et al., 2009; Olden and Naiman, 2010; A total of 521 specimens were captured. 127 females and
Paschoalini et al., 2013; Perini et al., 2013). It is known that 116 males from section 1, and 134 females and 144 males
alterations in the temperature and hydrological dynamics from section 2.
of rivers can negatively affect the reproductive activity and The fish were captured using gillnets with 3-6 cm
other biological processes of several freshwater fish with between opposite knots and were immediately
long-term deleterious effects in the aquatic community transported to the Integrated Center for Fisheries
(Arenzon et al., 2002). For example, the colder temperature Resources and Aquaculture of Três Marias – CODEVASF.
of the water downstream from reservoirs may affect the The specimen, if alive, were anesthetized with Eugenol
gonadal development, ovarian follicle diameter, fecundity (Fernandes et al., 2016) and then euthanized by transversal
and gonads growth in fish (Armstrong and Witthames, section of the cervical medulla, following the ethical
2012; Kolm and Ahnesjö, 2005). principles of animal handling established by the Brazilian
This type of impact on fish has already been reported College for Animal Experimentation (COBEA). For each
in rivers in others regions of the world, for example specimen, the following parameters were recorded: total
China (Yi et al., 2014) and French Guiana (Ponton, 1998). length (TL; accuracy: 1cm), body weight (BW; accuracy:
Recent studies in Brazil have shown that the reproduction 0.01g) and gonadal weight (GW; accuracy: 0.01g). Ten
of migratory and non-migratory small forage fishes was voucher specimens were sent to Natural Sciences Museum
negatively impacted in the first kilometers downstream of Pontifícia Universidade Católica de Minas Gerais, Brazil
from the Três Marias Dam, where the temperature and (MCNIP-0624, 0653, 0743).
dissolved oxygen of the water are lower in the summer
due to thermal stratification of the reservoir in this 2.2. Biological indices
period (Arantes et al., 2010; Domingos et al., 2012;
To determine the gonadal volume for mature males and
Normando et al., 2014; Thomé et al., 2012). However, these
females, the gonadosomatic index (GSI) was calculated
studies also showed that approximately 24 km downstream
(Gonadosomatic index – GSI = Gonadal weight /Body
from Três Marias Dam, after the confluence with Abaeté
weight x 100). Fulton’s condition factor (Fulton’s condition
River, the biotic and abiotic conditions of the water
become favourable to the reproduction of migratory and factor – K = Body weight/Total length3 x 100) (Lizama and
non-migratory species. Ambrosio, 2002) was also calculated to compare the health
Despite the fact that most studies are conducted with status of the males and females between sampling sections.
migratory fish, there are few studies on Neotropical rivers
that have assessed the effects of dams on the reproduction 2.3. Physical-chemical parameters of the water
of resident or non-migratory fish (Bazzoli et al., 2019; The physical and chemical parameters of the water from
Donaldson et al., 2008). The Acestrorhynchus lacustris the two sections of the São Francisco River were recorded
(Lütken, 1875), popularly known as dogfish, is a non- bimonthly (n=7), on the same day and same sections as
migratory species, inhabiting the Paraná and São Francisco fish sampling occurred. The following parameters were
Rivers basins, two important South American basins. measured, at 1.5 m depth, with a Horiba U-10 probe: pH,
This species can reach 27 cm (Menezes, 2003) and has temperature (°C), dissolved oxygen (mg/L) and electrical
an important ecological role in the food chain, serving as conductivity (µS/cm). The water flow (m3/s) values were
prey for large piscivorous fish and controlling small fish supplied by Companhia Energética de Minas Gerais (CEMIG).
populations (Hahn et al., 2000). Additionally, A. lacustris
presents a long reproductive period and batch fecundity, 2.4. Gonadal maturation stages and follicular diameter
reproducing throughout the year (Godinho et al., 2009).
To assess de seasonal variation in reproductive activity,
Given the ecological importance of this species and the
the gonadal maturation stages of males and females
lack of studies focusing in reproductive biology of non-
were determined bimonthly through the macro and
migratory species influenced by dams, the present study
microscopic features of gonads and the changes in the
aimed to assess the seasonal variation in reproductive
gonadosomatic index according to Carvalho et al. (2009).
activity and how the alterations in water parameters
For microscopic analyses, gonad fragments of all specimens
downstream Três Marias Dam influence the reproduction
captured were previously fixed in Bouin’s solution and
of A. lacustris from São Francisco River, a very important
subsequently submitted to histological routine, embedding
river in Neotropical region.
in paraffin, 5 µm thick microtome sections and staining
in haematoxylin-eosin (HE).
The diameters of 50 vitellogenic follicles (DVF) were
2. Materials and Methods
obtained from mature ovaries of 10 specimens from each
sampling section, using an ocular micrometer attached
2.1. Sampling to a light microscope. Only intact vitellogenic follicles,
with little shrinkage and with the nucleus visible were
The specimens were captured, bimonthly, between May
measured (Arantes et al., 2010).
2011 and June 2012 in two sections of the São Francisco
River: section 1, immediately downstream of Três Marias
Dam (18°09’31.65”S and 45°13’36.00”W) and section 2, 2.5. Fecundity
downstream of confluence of São Francisco and Abaeté In order to determine the batch fecundity, samples from
River (18°02’47.78”S and 45°10’57.95”W) (see Figure 1). the middle region of 20 mature females from each section

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Dam affecting non-migratory fish

Figure 1. Sampling sections of the São Francisco River, downstream from Três Marias Dam. Section 1: immediately downstream the
Dam; Section 2: immediately after the confluence with Abaeté River. UTM coordinates.

were fixed in modified Gilson’s solution (100 ml of 60% water parameters and the Mann-Whitney to compare
ethanol, 880 ml ​​distilled water, 15 ml of 80% nitric acid, biological data. For the comparison between sizes classes
18 ml of glacial acetic acid and 20g of mercury chloride) of vitellogenic follicles, we used the Kruskal-Wallis test
until the complete dissociation of the follicles. With the followed by the post hoc Dunn test.
aid of a stereoscopic microscope, the vitellogenic follicles Biometric data, GSI, fecundity, vitellogenic follicle
were separated from the others by their opaque colour diameters, maturation stages and abiotic factors are
and counted. The batch fecundity (BF) was determined expressed in tables and graphs with mean ± standard
by the expression: BF= VF×GW, in which VF = number of deviation (SD). A significance level of p <0.05 was used
vitellogenic follicles per ovary gram and GW= gonadal for all analysed tests. Statistical analyses and graphs were
weight (Melo et al., 2011). Relative fecundity with body done by software GraphPad Prism 7.0 for windows.
weight was estimated by the expression: RF= BF/BW, where
BF= batch fecundity, BW= body weight.
3. Results
2.6. Statistical analyses
We conducted the Lilliefors test for all studied
parameters in order to determine the normality of 3.1. Physical and chemical parameters of the water
data. Then, to analyse the variables between sections, The physical and chemical parameters analysed
we used the T-student test for physical and chemical showed that the temperature, dissolved oxygen and

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Gomes, R.Z. et al.

flow presented higher mean values ​​in section 2, with 3.3. Gonadal maturation stages
significant statistical differences in relation to the values ​​of The following macro and microscopic features of each
section 1. However, electrical conductivity and pH showed maturation stages were identified for females: resting –
no statistical difference between sections (see Table 1). F1= thin, translucent and less vascularised ovaries with

3.2. Biometry, biological indices and fecundity


Regarding to total length and body weight, females
and males did not show statistical variations between
sections 1 and 2. The GSI (mean ± SD) of mature females
and males presented statistical differences between
sections. On the other hand, Fulton’s condition factor
did not show significant difference between sampling
sections for both sexes (as shown in Tables 2 and 3). The
batch fecundity (BF) also presented significant statistical
differences between sampling sections, showing high
values in female fish from section 2 (as shown in Table 2).
The vitellogenic follicles of A. lacustris collected had
an average diameter of 733.6 ± 52.7 µm in section 1 and
786.1 ± 65.9 µm in section 2, with statistical difference
between them (as shown in Table 2). It was determined Figure 2. Frequency (%) and size classes of vitelogenic follicles (µm)
four size classes of vitellogenic follicles of this species of A. lacustris from fully grown ovaries of A. lacustris. Different bar
and size class with the highest number of follicles was colours indicate statistically significant differences between the
700-860 µm (see Figure 2). diameter classes (p< 0.05).

Table 1. Physical and chemical parameters of two sampled sections downstream Três Marias Dam, São Francisco River.

Section 1 Section 2
Mean ± SD Range Mean ± SD Range
Temperature (oC) 23.21 ± 0.57a 22.68-24.00 24.31 ± 0.71b 23.58-25.40
Dissolved Oxygen (mg/L) 5.55 ± 1.67a 4.13-8.12 7.97 ± 0.55b 7.33-8.65
pH (Sorensen) 5.83 ± 0.46a 5.12-6.24 6.35 ± 0.51a 5.62-7.02
Electrical conductivity (µS/cm) 68.6 ± 1.5a 67.00-71.00 64.2 ± 7.19a 56.00-74.00
Flow (m3/s) 693.22 ± 100.58a 584.93-798.22 815.13 ±52.71b 724.57-854.51
Different letters indicate statistical difference between sections (p<0.05). SD= standard deviation.

Table 2. Biological and reproductive data of A. lacustris females in two sections of São Francisco River.

Females Section 1 Section 2


N 127 134
Mean ± SD Range Mean ± SD Range
TL (cm) 20.69 ± 1.76a 14.2-24.8 21.01 ± 2.4a 14.4-25.9
BW (g) 80.24 ± 27.9a 25.8-158 86.65 ± 28.9a 24.4-135.0
GSI (%) 2.92 ± 0.76a 0.98-3.89 4.37 ± 1.12b 3.0-7.1
FD (µm) 733.6 ± 52.75a 622.6-822.4 786.1 ± 65.96b 702.2-925.2
BF 2,587 ± 911a 996-4,809 4,179 ± 1,889b 2,156-7,854
K 0.96 ± 0.20a 0.63-2.9 0.93 ± 0.11a 0.65-1.25
Different letters indicate statistical difference between sections (p<0.05). N= number of individuals; SD= standard deviation; TL= total length;
BW= body weight; GSI= gonadosomatic index; FD= Follicular diameter; BF= Batch fecundity; K= Fulton’s condition factor.

Table 3. Biological and reproductive data of A. lacustris males in two sections of São Francisco River.

Males Section 1 Section 2


N 116 144
Mean ± SD Range Mean ± SD Range
TL (cm) 16.6 ± 1.4a 14.0-21.0 16.9 ± 1.5a 13.8-20.8
BW (g) 39.5 ± 14.4a 15.0-85 40.8 ± 12.7a 20.0-90.0
GSI (%) 0.64 ± 0.29a 0.03-1.0 1.01 ± 0.48b 0.43-2.37
K 0.86 ± 0.10a 0.51-1.1 0.84 ± 0.09a 0.69-1.20
Different letters indicate statistical difference between sections (p<0.05). N= number of individuals; SD= standard deviation; TL= total length;
BW= body weight; GSI= gonadosomatic index; K= Fulton’s condition factor.

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Figure 3. Ovaries in different maturation stages and the respective transversal sections stained by HE. (A) resting, (B) initial maturation,
(C) advanced maturation/mature, (D) partially spawned, (E) totally spawned ovaries, (F) post-ovulatory follicle, (G) yellow body. O1= early
perinucleolar follicles; O2= late perinucleolar follicles; O3= pre-vitellogenic follicles; O4= vitellogenic follicles; POF= post-ovulatory
follicle; YB= yellow body. Scales bars represent 100 µm.

initial follicles (O1) and advanced (O2) perinucleolar (see and presenting the lumen of seminiferous tubules filled
Figure 3A); initial maturation - F2= voluminous, orange with spermatozoa (see Figure 4B); partially spent - M4A=
ovaries, and histologically containing initial perinucleolar testicles are flaccid, haemorrhagic, with translucent and
follicles (O1), advanced perinucleolar follicles (O2) and milky-white areas, seminiferous tubules’ lumen partially
pre-vitellogenic follicles (O3) (see Figure 3B); advanced empty, containing few spermatozoa (see Figure 4C). Resting -
maturation/mature - F3= ovaries of maximum volume, with M1 and totally spent males -M4B were not captured in
numerous vitellogenic follicles (O4) visible to the naked present study.
eye, dark brown in colour, besides having follicles at all
developmental stages (see Figure 3C); partially spawned 3.4. Reproductive activity
- F4A= flaccid, haemorrhagic ovaries with follicles at all
Females and males in reproductive activity, stages 2,
developmental stages, besides post-ovulatory follicles
(see Figure 3D-F) and totally spawned ovaries - F4B= very 3, and 4A, were recorded throughout the year in both
flaccid and haemorrhagic, histologically containing O1, O2, sampling sections. The long reproductive period and the
and final atretic follicles (see Figure 3E-G). presence of partially spawned females with post-ovulatory
For males, the following macro and microscopic features follicles and follicles in all developmental stages indicate
of each maturation stages were identified: initial maturation that the species present batch spawning of the multiple
- M2= whitish testicles, containing a small amount of type. In section 1, 66% of females and 29% of males were
spermatozoa and seminiferous tubules wall with cysts in advanced maturation stage. In section 2, 49% of females
of spermatogenic cells in all developmental stages (see and 24% of males were in advanced maturation. In general,
Figure 4A); advanced maturation/mature - M3= testicles this species presented reproductive activity in both sampled
reach the maximum volume, are milky-white in colour sections (as shown in Figure 5).

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Gomes, R.Z. et al.

between the two sections. The standardization of the


sample in the same size class, generates greater reliability
of the data in the comparative studies, since in fish several
reproductive parameters can be influenced by weight
and length, such as fecundity, follicle diameter, gonadal
volume and sperm production (Benejam et al., 2010;
Muchlisin et al., 2011; Paschoalini et al., 2019).
Acestrorhynchus lacustris from both sections presented
reproductive activity concentrated in the spring and
summer, however the presence of mature specimens in all
seasons was detected, a common feature for non-migratory
fish from tropical environments (Lowe-McConnell, 1987).
This species showed reproductive activity during almost the
whole year as observed by Bazzoli and Godinho (1991) who
studied the reproductive biology of the same species in a
lentic environment, i.e. Três Marias reservoir. Similar to our
data, the absence of the resting and fully spent males was
also noted in a lentic environment (Bazzoli and Godinho,
1991), which may be indicative of a fast gonad recovery
(recrudescence period) in dogfish males (Rinchard and
Kestemont, 1996). In females of A. lacustris, four diameter
classes of vitellogenic follicle were observed, indicating
an asynchronous folliculogenesis and corroborating with
observations in other non-migratory teleost (Armstrong
and Witthames, 2012; Bazzoli et al., 2019; Melo et al., 2011).
Fish with these characteristics generally have greater
biological plasticity, greater tolerance to variations in the
environmental conditions when compared to fish with
seasonal reproductive activity, such as the migratory species
(Campos-Mendoza et al., 2004; Godinho et al., 2009;
Sato et al., 2005; Thomé et al., 2012). However, in present
Figure 4. Testis in different maturation stages and respective study we detected some alterations in reproductive
transversal sections stained by HE. (A) early maturation, (B) parameters of A. lacustris in both sexes from section 1.
advanced maturation/mature, (C) partially spent; Z= spermatozoa; The Fulton’s condition factor and GSI are frequently
C2= secondary spermatocytes T= spermatids; ST= seminiferous used to asses environmental quality, since the body
tubules. Scale bars represent A= 100 µm, B= 200 µm and C= 500 µm. growth and gonads development can be influenced by the
environmental conditions (Thomé et al., 2012; Yoda and
Yoneda, 2009). Fulton’s condition factor is derived from
4. Discussion the consideration that for a group of individuals of the
same size, those weighing more are in better condition
The results of this study suggest that the alterations (Abujanra et al., 2009). However, in the present study no
in water parameter immediately downstream of Três significant differences was observed in the weight and
Marias Dam influence the reproductive potential of size of males and females from both sections, a fact that
a non-migratory fish A. lacustris. This influence has may explain the absence of significant difference in the
already been shown by other authors studying migratory condition factor. On the other hand, we observed statistical
species (Sato et al., 2005; Thomé et al., 2012) and small differences in mean values of GSI between fish from the two
forage fish (Normando et al., 2014). However, unlike sections analysed. The highest growth of the ovaries and
migratory and forage fishes, A. lacustris maintained the testicles of fish from section 2 is similar to that observed for
reproductive activity, even with different performance, in migratory species in the same study area (Sato et al., 2005;
both sections analysed in São Francisco River. Similar to Arantes et al., 2010; Weber et al., 2013). Furthermore, in
our results, the impacts in aquatic organisms due to females was observed lower size in the vitellogenic follicle
the release of colder water, with low concentration of diameter of fish caught in section 1, corroborating that
dissolved oxygen, were also detected in others dammed observed by Sato et al. (2005) and Arantes et al. (2010) in a
rivers, such as: Serrasalmus brandtii from São Francisco total spawning Neotropical species; Normando et al. (2014)
River, Brazil (Bazzoli et al., 2019); aquatic invertebrate in non-migratory forage species; and Bazzoli et al. (2019)
community from South African Rivers (Mantel et al., 2010); in others non-migratory species. The vitellogenic follicle
and other several fish species in USA rivers (Graf, 2006; diameter is reported as an important parameter related
Donaldson et al., 2008). to reproductive fitness because larger follicles produce
Regarding to biometry results, no significant differences offspring with more energy reserves (Kinnison et al., 1998;
in weight and length of the specimens was observed Kolm and Ahnesjö, 2005; Lubzens et al., 2010).

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Figure 5. Frequency of the maturation stages of the A. lacustris collected in two sections on the São Francisco River downstream from
the Três Marias Dam. Gonadal maturation stages of females: F1= resting, F2= initial maturation, F3= advanced maturation/mature,
F4A= partially sapawned and F4B= totally sapawned; and males: M2= initial maturation, M3= advanced maturation/mature and
M4A= partially spent.

Fecundity is reported as a parameter which is strongly reproductive strategy, presented reproductive parameters
linked to the environmental conditions (Armstrong and altered in the section 1 downstream from the Três Marias
Witthames, 2012). Food availability and water temperature Dam, where the physical and chemical conditions of the
are reported as major factors capable of influencing the water are unfavourable to fish reproduction. In both sexes
reproductive potential through the number and diameter was noted a decrease in gonadal volume, and females
of vitellogenic follicles (Armstrong and Witthames, 2012; showed lower values of follicle diameter and fecundity,
Kinnison et al., 1998; Yoda and Yoneda, 2009). In the present when compared to section 2, confirming that the impact
study, batch fecundity showed statistically differences
of dams also occurs on non-migratory fish.
between fish collected from the two sampling sections,
indicating that the number of vitellogenic follicles in ovaries
was negatively affected by the water conditions in section 1.
Acknowledgements
In an integrated analysis of the results, our data showed that
unlike migratory species (Arantes et al., 2010; Perini et al., 2013), The authors thank the partnership of CEMIG-GT/
the non-migratory species A. lacustris, maintain their CODEVASF. This work had the financial support of the
reproductive activity even in environments with lower Coordenação de Aperfeiçoamento de Pessoal de Nível
temperature, dissolved oxygen and flow, suggesting a greater Superior (CAPES) under grant (Finance code-001); Conselho
tolerance for environmental changes than migratory fish.
Nacional de Desenvolvimento Científico e Tecnológico
However, even though it is considered a more resistant species,
(CNPq) under grant (306946/2016-5 and 407719/2016-4);
these alterations in the physical and chemical parameters of
and Fundação de Amparo à Pesquisa do Estado de Minas
water reflected the decrease in the reproductive fitness of
Gerais (FAPEMIG) under grant (APQ03232-15).
this species, fact that may influence in a worse health status
of the offspring and affect the maintenance and conservation
of this species in the São Francisco River.
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